Social instability stress in adolescent male rats alters hippocampal neurogenesis and produces deficits in spatial location memory in adulthood

Hippocampus

Volumn 22, Issue 6, 2012, Pages 1300-1312

  McCormick, Cheryl M ^a   Thomas, Catherine M ^a   Sheridan, Cheryl S ^a   Nixon, Feather ^a   Flynn, Jennifer A ^a   Mathews, Iva Z ^a  

^a BROCK UNIVERSITY   (Canada)

Author keywords

Calcium calmodulin dependent kinase II; Doublecortin; Ki67; Microglia; Synaptophysin

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE II; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; IMMUNOCOMPETENT CELL; MALE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SOCIAL INSTABILITY STRESS; SOCIAL STRESS; SPATIAL MEMORY;

AGE FACTORS; ANIMALS; HIPPOCAMPUS; INTERPERSONAL RELATIONS; MALE; MEMORY; MEMORY DISORDERS; NEUROGENESIS; RANDOM ALLOCATION; RATS; RATS, LONG-EVANS; SPATIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 84861341664     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20966     Document Type: Article

References (78)

1. Abe H, Ishida Y, Nonaka H, Iwasaki T. 2009. Functional difference between rat perirhinal cortex and hippocampus in object and place discrimination tasks. Behav Brain Res 197: 388-397.
2. Aggleton J, Hunt P, Rawlins J. 1986. The effects of hippocampal lesions upon spatial and non-spatial tests of working memory. Behav Brain Res 19: 133-146.
3. Aldridge GM, Podrebarac DM, Greenough WT, Weiler IJ. 2008. The use of total protein stains as loading controls: An alternative to high-abundance single-protein controls in semi-quantitative immunoblotting. J Neurosci Methods 172: 250-254.
4. Anagnostaras SG, Gale GD, Fanselow MS. 2001. Hippocampus and contextual fear conditioning: Recent controversies and advances. Hippocampus 11: 8-17.
5. Avital A, Richter-Levin G. 2005. Exposure to juvenile stress exacerbates the behavioural consequences of exposure to stress in the adult rat. Int J Neuropsychopharmacol 8: 163-173.
6. Balu DT, Lucki I. 2009. Adult hippocampal neurogenesis: Regulation, functional implications, and contribution to disease pathology. Neurosci Biobehav Rev 33: 232-252.
7. Barha C, Brummelte S, Lieblich SE, Galea LAM. Chronic restraint stress in adolescence differentially infliuences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus (in press).
8. Bessis A, Bechade C, Bernard D, Roumier A. 2007. Microglial control of neuronal death and synaptic properties. Glia 55: 233-238.
9. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. 2003. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467: 1-10.
10. Burke AR, Renner KJ, Forster GL, Watt MJ. 2010. Adolescent social defeat alters neural, endocrine and behavioral responses to amphetamine in adult male rats. Brain Res 1352: 147-156.
11. Cameron HA, McKay RDG. 2001. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435: 406-417.
12. Colbran RJ. 2004. Protein phosphatases and calcium/calmodulin-dependent protein kinase II-dependent synaptic plasticity. J Neurosci 24: 8404-8409.
13. Conrad CD. 2008. Chronic stress-induced hippocampal vulnerability: The glucocorticoid vulnerability hypothesis. Rev Neurosci 19: 395-411.
14. Conrad CD, Magariños AM, LeDoux JE, McEwen BS. 1999. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 113: 902-913.
15. Dagyte G, Van der Zee E, Postema F, Luiten PG, Den Boer JA, Trentani A, Meerlo P. 2009. Chronic but not acute footshock stress leads to temporary suppression of cell proliferation in rat hippocampus. Neuroscience 162: 904-913.
16. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. 2003. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460: 563-572.
17. Dobrossy MD, Drapeau E, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. 2003. Differential effects of learning on neurogenesis: Learning increases or decreases the number of newly born cells depending on their birth date. Mol Psychiatr 8: 974-982.
18. Dupret D, Fabre A, Dobrossy MD, Panatier A, Rodriguez JJ, Lamarque S, Lemaire V, Oliet SHR, Piazza PV, Abrous DN. 2007. Spatial learning depends on both the addition and removal of new hippocampal neurons. Plos Biol 5: 1683-1694.
19. Ekdahl CT, Kokaia Z, Lindvall O. 2009. Brain inflammation and adult neurogenesis: The dual role of microglia. Neuroscience 158: 1021-1029.
20. Ennaceur A, Delacour J. 1988. A new one-trial test for neurobiological studies of memory in rats. I. Behavioral data. Behav Brain Res 31: 47-59.
21. Ennaceur A, Meliani K. 1992. A new one-trial test for neurobiological studies of memory in rats. III. Spatial vs. Non-spatial working memory. Behav Brain Res 51: 83-92.
22. Ennaceur A, Neave N, Aggleton JP. 1997. Spontaneous object recognition and object location memory in rats: The effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 113: 509-519.
23. Epp JR, Haack AK, Galea LAM. 2011. Activation and survival of immature neurons in the dentate gyrus with spatial memory is dependent on time of exposure to spatial learning and age of cells at examination. Neurobiol Learn Mem 95: 316-325.
24. Fanselow MS, Dong HW. 2010. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65: 7-19.
25. Gerges NZ, Aleisa AM, Schwarz LA, Alkadhi KA. 2004. Reduced basal camkii levels in hippocampal ca1 region: Possible cause of stress-induced impairment of ltp in chronically stressed rats. Hippocampus 14: 402-410.
26. He J, Crews FT. 2007. Neurogenesis decreases during brain maturation from adolescence to adulthood. Pharmacol Biochem Behav 86: 327-333.
27. Heine VM, Maslam S, Zareno J, Joels M, Lucassen PJ. 2004. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci 19: 131-144.
28. Hodes GE, Shors TJ. 2005. Distinctive stress effects on learning during puberty. Horm Behav 48: 163-171.
29. Howland JG, Wang YT. 2008. Synaptic plasticity in learning and memory: Stress effects in the hippocampus. Prog Brain Res 169: 145-158.
30. Isgor C, Kabbaj M, Akil H, Watson SJ. 2004. Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats. Hippocampus 14: 636-648.
31. Jurgens HA, Johnson RW. Dys-regulated neuronal-microglial cross-talk during aging, stress and inflammation. Exp Neurol (in press).
32. Kee N, Sivalngam S, Bonnstra R, Wojtowicz JM. 2002. The utility of Ki-67 and BRDU as proliferative markers of adult neurogenesis. J Neurosci Methods 115: 97-105.
33. Kesner RP, Lee I, Gilbert P. 2004. A behavioral assessment of hippocampal function based on a subregional analysis. Rev Neurosci 15: 333-351.
34. Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS. 2000. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: Role of microglia. J Neurosci 20: 6309-6316.
35. Konradi CL. 2003. Quantification of protein in brain tissue by western immunoblot analysis. Methods Mol Med 79: 263-271.
36. Luine V, Villegas M, Martinez C, McEwen BS. 1994. Repeated stress causes reversible impairments of spatial memory performance. Brain Res 639: 167-170.
37. Madsen TM, Kristjansen PEG, Bolwig TG, Wortwein G. 2003. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119: 635-642.
38. Maggio N, Segal M. 2011. Persistent changes in ability to express long-term potentiation/depression in the rat hippocampus after juvenile/adult stress. Biol Psychiatr 69: 748-753.
39. Mathews IZ, Wilton A, Styles A, McCormick CM. 2008. Heightened neuroendocrine function in males to a heterotypic stressor and increased depressive behaviour in females after adolescent social stress in rats. Behav Brain Res 190: 33-40.
40. Mathieu P, Battista D, Depino A, Roca V, Graciarena M, Pitossi F. 2010. The more you have, the less you get: The functional role of inflammation on neuronal differentiation of endogenous and transplanted neural stem cells in the adult brain. J Neurochem 112: 1368-1385.
41. McCormick CM. 2010. An animal model of social instability stress in adolescence and risk for drugs of abuse. Physiol Behav 99: 194-203.
42. McCormick CM, Mathews IZ. 2010. Adolescent development, hypothalamic-pituitary-adrenal function, and programming of adult learning and memory. Prog Neuro-Psychopharm Biol Psychiatr 34: 756-765.
43. McCormick CM, Robarts D, Kopeikina K, Kelsey JE. 2005. Long-lasting, sex-and age-specific effects of social stress on corticosterone responses to restraint and locomotor responses to psychostimulants in rats. Horm Behav 48: 64-74.
44. McCormick CM, Merrick A, Secen J, Helmreich DL. 2007. Social instability in adolescence alters the central and peripheral hypothalamic-pituitary-adrenal responses to a repeated homotypic stressor in male and female rats. J Neuroendocrinol 19: 116-126.
45. McCormick CM, Smith C, Mathews IZ. 2008. Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res 187: 228-238.
46. McCormick CM, Mathews IZ, Thomas C, Waters P. 2010a. Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models. Brain Cogn 72: 73-85.
47. McCormick CM, Nixon F, Thomas C, Lowie B, Dyck J. 2010b. Hippocampal cell proliferation and spatial memory performance after social instability stress in adolescence in female rats. Behav Brain Res 208: 23-29.
48. McEwen BS. 2010. Stress, sex and neural adaptation to a changing environments: Mechanisms of neuronal remodeling. Ann NY Acad Sci 1204: E38-E59.
49. McEwen BS, Sapolsky RM. 1995. Stress and cognitive function. Curr Opin Neurobiol 5: 205-216.
50. Mirescu C, Gould E. 2006. Stress and adult neurogenesis. Hippocampus 16: 233-238.
51. Morrissey MD, Mathews IZ, McCormick CM. 2011. Enduring deficits in contextual and auditory fear conditioning after adolescent, not adult, social instability stress in male rats. Neurobiol Learn Mem 95: 46-56.
52. Mumby DG, Gaskin S, Glenn MJ, Schramek TE, Lehmann H. 2002. Hippocampal damage and exploratory preferences in rats: Memory for objects, places, and contexts. Learn Mem 9: 49-57.
53. Pavlides C, Nivon LG, McEwen BS. 2002. Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 12: 245-257.
54. Paxinos G, Watson C. 2005. The Rat Brain in Stereotaxic Coordinates. Sydney: Elsevier.
55. Phillips RG, LeDoux JE. 1992. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106: 274-285.
56. Pi HJ, Otmakhov N, Lemelin D, De Koninck P, Lisman J. 2010. Autonomous camkii can promote either long-term potentiation or long-term depression, depending on the state of t305/t306 phosphorylation. J Neurosci 30: 8704-8709.
57. Pohl J, Olmstead MC, Wynne-Edwards KE, Menard JL. 2007. Repeated exposure to stress across the childhood-adolescent period alters rats' anxiety- and depression-like behaviors in adulthood: The importance of stressor type and gender. Behav Neurosci 121: 462-474.
58. Pollak DD, Herkner K, Hoeger H, Lubec G. 2005. Behavioral testing upregulates pCamkII, BDNF, psd-95 and egr-1 in hippocampus of fvb/n mice. Behav Brain Res 163: 128-135.
59. Romeo RD. 2010. Pubertal maturation and programming of hypothalamic-pituitary-adrenal reactivity. Front Neuroendocrinol 31: 232-240.
60. Saxe MD, Battaglia F, Wang JW, Malleret G, David DJ, Monckton JE, Garcia ADR, Sofroniew MV, Kandel ER, Santarelli L, Hen R, Drew MR. 2006. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci USA 103: 17501-17506.
61. Scharfman HE, Hen R. 2007. Is more neurogenesis always better? Science 315: 336-338.
62. Schmitt U, Tanimoto N, Seeliger M, Schaeffel F, Leube RE. 2009. Detection of behavioral alterations and learning deficits in mice lacking synaptophysin. Neuroscience 162: 234-243.
63. Scholzen T, Gerdes J. 2000. The ki-67 protein: From the known and the unknown. J Cell Physiol 182: 311-322.
64. Shors TJ, Townsend DA, Zhao MR, Kozorovitskiy Y, Gould E. 2002. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12: 578-584.
65. Sousa N, Lukoyanov NV, Madeira MD, Almeida OFX, Paula-Barbosa MM. 2000. Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97: 253-266.
66. Spencer JL, Waters EM, Romeo RD, Wood GE, Milner TA, McEwen BS. 2008. Uncovering the mechanisms of estrogen effects on hippocampal function. Front Neuroendocrinol 29: 219-237.
67. Sterlemann V, Rammes G, Wolf M, Liebl C, Ganea K, Muller MB, Scmidt MV. 2010. Chronic social stress during adolescence induces cognitive impairment in aged mice. Hippocampus 20: 540-549.
68. Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, Mortrud MT, Cusick A, Riley ZL, Sunkin SM, Bernard A, Puchalski RB, Gage FH, Jones AR, Bajic VB, Hawrylycz MJ, Lein ES. 2008. Genomic anatomy of the hippocampus. Neuron 60: 1010-1021.
69. Toth E, Avital A, Leshem M, Richter-Levin G, Braun K. 2008. Neonatal and juvenile stress induces changes in adult social behavior without affecting cognitive function. Behav Brain Res 190: 135-139.
70. Wang HM, Hu YG, Tsien JZ. 2006. Molecular and systems mechanisms of memory consolidation and storage. Prog Neurobiol 79: 123-135.
71. Watt MJ, Burke AR, Renner KJ, Forster GL. 2009. Adolescent male rats exposed to social defeat exhibit altered anxiety behavioral and limbic monoamines as adults. Behav Neurosci 123: 564-576.
72. Weintraub A, Singaravelu J, Bhatnagar S. 2010. Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Res 1343: 83-92.
73. Weitzdorfer R, Hoger H, Shim KS, Cekici L, Pollak A, Lubec G. 2008. Changes of hippocampal signaling protein levels during postnatal brain development in the rat. Hippocampus 18: 807-813.
74. Winters BD, Forwood SE, Cowell RA, Saksida LM, Bussey TJ. 2004. Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: Heterogeneity of function within the temporal lobe. J Neurosci 24: 5901-5908.
75. Wright LD, Hebert KE, Perrot-Sinal TS. 2008. Periadolescent stress exposure exerts long-term effects on adult stress responding and expression of prefrontal dopamine receptors in male and female rats. Psychoneuroendocrinology 33: 130-142.
76. Yildirim M, Mapp OM, Janssen WGM, Yin WL, Morrison JH, Gore AC. 2008. Postpubertal decrease in hippocampal dendritic spines of female rats. Exper Neurol 210: 339-348.
77. Yirmiya R, Goshen I. 2011. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 25: 181-213.
78. Zhao CM, Deng W, Gage FH. 2008. Mechanisms and functional implications of adult neurogenesis. Cell 132: 645-660.